Epigenetic regulation of the sex determination gene megi in polyploid persimmon

Abstract

Epigenetic regulation can add a flexible layer to genetic variation, potentially enabling long-term but reversible cis-regulatory changes to an allele while maintaining its DNA sequence. Here, we present a case in which alternative epigenetic states lead toreversible sex determination in the hexaploid persimmon Diospyros kaki. Previously, we elucidated the molecular mechanismof sexdetermination in diploid persimmon and demonstrated the action of a Y-encoded sex determinant pseudogene called OGI, whichproduces small RNAs targeting the autosomal gene MeGI, resulting in separate male and female individuals (dioecy). We contrastthese findings with the discovery, in hexaploid persimmon, of an additional layer of regulation in the form of DNA methylation of theMeGI promoter associated with the production of both male and female flowers in genetically male trees. Consistent with this model, developing male buds exhibited higher methylation levels across the MeGI promoter than developing female flowers from either monoecious or female trees. Additionally, a DNA methylation inhibitor induced developing male buds to form feminized flowers. Concurrently, in Y-chromosome-carrying trees, the expression of OGI is silenced by the presence of a SINE (short interspersed nuclear element)-like insertion in the OGI promoter. Our findings provide an example of an adaptive scenario in volving epigenetic plasticity.